Evidence That the Forebrain is Responsible for Strategic Actions

by David D. Olmsted (Copyright - 2000, 2006. Free to use for personal and
educational purposes)
Last Revised September 4, 2006

Introduction

The forebrain (telencephalon) seems to have the purpose of motivating the animal
to seek its ideal surroundings. While the hypothalamus motivates the animal
based upon its internal state the forebrain via its septum and amygdala motivates
the animal based upon its percieved external state. As such it governs the animal's
strategic actions as opposed to its targeted tactical actions governed by the tectum
region located at the other end of the hypothalamus.. With this purpose one can
see the evolutionary pressures that lead to its further development into the primate
neocortex and sub-cortical structures.

Removal of the Forebrain Affects Activity Levels and Strategic Learning

In 1912 Theodore Burnett at the University of California tested frogs with and without
their forebrain (cerebral cortex, septum, amygdala) in the testing apparatus
known as the labyrinth shown below in figure 1.

Figure 1 The Labyrinth (Burnett - 1912)

Burnett had this to say about these frogs (two Rana pipiens and one Rana
boylii):

"Any one casually observing
a decerebrate frog would say there was no difference between such a frog and a normal
one. But if a normal and a decerebrate frog are observed at the same time
it will be seen that there is a difference of degree. The decerebrate frog
is somewhat less spontaneous. When a normal and a decerebrate frog were put
in the labyrinth together the normal frog would at once start forward in his effort
to escape. The decerebrate frog, however, would remain quiet for varying lengths
of time before it would start forward. This was rather a drawback to the experiments
in the labyrinth as it required constant stimulation to keep the decerebrate
frogs moving."

"It was also noticed that the decerebrate frogs spent a great
deal more time in the water than did the normal. On several occasions they were
taken from the water and placed with the normal frogs. Sometimes they would jump
back again without any apparent cause; at other times the slamming of a door or
the jarring of the building would be followed by a "plump" as the decerebrate
frogs jumped into the water. If a decerebrate frog happened to be 'sitting on the
bank', so to speak, and one approached suddenly or made a sudden gesture it
would immediately spring into the water, especially if oriented in that direction.
If oriented in some other direction the frog might turn but more likely it would
spring forward, come into contact with the wall of its habitat, turn, and take to
the water. The normal frog, on the contrary, was just as likely to crouch and remain
perfectly motionless."

While in the their cage these decerebrate frogs were not
able to acquire sufficient food so everyday each one was placed in a glass jar along
with many one winged flies and they remained there until all the flies had
been eaten. While in a glass
jar a decerebrate frog typically remained motionless until a fly came into
its field of view. It then turned its head and if the fly kept moving the frog would spring and snap. If the fly stopped nothing would happen.

The question which Burnett sought to answer was whether a decerebrate
frog like a normal frog could learn a path of escape from an unpleasant situation
in the labyrinth. The answer was that it could not as explained below:

"As soon
as he (a normal frog) entered the labyrinth a drop of ether was let fall upon
his back. The frog lost no time in moving on, but went in a straight line
to the right side which was closed with glass. Single induction shocks were then
sent through the wires, whereupon the frog whirled about and jumped off to
the clear space. After sitting quietly for a few minutes he went to the open
end and escaped. After about twenty trials this normal frog would make his escape
with rarely an error. Occasionally he would make a mistake and go to the glass,
but would correct the error on feeling the first shock. In order to be sure
this was an association the labyrinth was reversed, the left opening being closed
by a glass plate. The frog went straight to the left side as usual and finding his
way blocked, tried to 'bore' through the glass. An induction shock was followed
by violent efforts to escape through the glass until finally a sudden turn
and jump sent him towards the rear end. After sitting for a short time the
frog went to the rear end of the labyrinth whence he started. It was quite obvious
that he was at a loss how to escape."

"The decerebrate frogs behaved in a very different
manner. On entering the labyrinth they would jump forward when stimulated by the
ether and generally landed on the wires in the middle of the passage. If the induction
shock was weak they would either jump a short distance or crawl forward a short
distance. If the current was strong they would give a spring forward and land
at the glass, or if oriented toward the open end, as often happened, they
would spring to the opening and escape. If stimulated at the glass end they
would make frantic efforts to get through or over the glass, until falling backward,
they would be oriented toward the rear of the labyrinth. They would then go to the
rear end, only to be made uncomfortable by the ether, when back they would
go again to the glass."

Over one hundred trails were made with Rana boylii with
no improvement in its escape ability.

An Example of Strategic Behavior - Seeking
Out Light so as to Catch Bugs

During the winter (October to February) 1902-03
Ellen Torelle at Bryn Mawr looked at the light responses of two species of
frogs, Rana virescens and Rana
clamata. The frogs were placed in boxes twelve
inches long, five inches high, and nine inches wide having a glass window
at one end and a door at the other. The inside of the box was painted black.

Response to Diffuse Light at Laboratory Temperature

Frogs were placed at
the dark end of the box with their heads pointed away from the light. They
usually took 1/4 to 1 minute to reach the light after which they remained at that
end looking out.

Response to Direct Light at Laboratory Temperature

"The sunlight
fell into one end of the box only. In each case the response was immediate
and positive. The animals moved directly to the illuminated end of the box,
where they remained a variable length of time, from two to four minutes, when
they moved backward, just outside the circle of bright illumination, where they
remained until taken away, the median plane of the body being parallel to
the incoming ray. In most cases, when the sun illuminated area was small,
the head was not turned from the light during the retreat, which was accomplished
by moving first one side of the body, then the other, sidewise and backward.
In other cases the frogs turned at right angles to the light, hopped outside
the area of intense illumination, and oriented themselves with their heads
in the direction of the incoming ray."

"Since the retreat into the area of less
intense illumination might have been caused by the heat of the sun's rays, the experiments
were repeated, heat being cut off by placing a glass vessel ...filled with water
close to the glass end of the box. In each case the result was practically
the same as before."

Response to Direct Light Outside

Frogs were carried
outside on a plate covered by by an opaque bell jar.

"It was deposited three
yards from the shadow of the building, the bell jar removed and the
frog left on the plate with its head turned away from the sun and from the shadow
of the building. The frog first hopped forward, then stopped, turned in the
direction of the sun, and hopped well into the shadow where it remained quietly
for ten minutes. It was then moved into the sunshine in about its former position.
Again it turned and hopped into the shadow. The results were very much the
same in the case of each frog tried."

What one seems to have here is movement to
the optimum area for catching bugs. Frogs in the shade are partly hidden and
not subject to overheating and drying out. In contrast the bugs are illuminated
by the sun and stand out with high contrast.

Orientation with One Eye Covered

A hood was attached to the head of a frog such that the left eye was covered
and the frog placed in the dark end of the box.

"It immediately turned with
its right eye directed toward the source of light, i.e. with its body oblique
to the incoming ray. The angle of deviation from the direction of the incoming
ray differed in different individuals. Five frogs were tried, but in no case
was the orientation that observed when both eyes were covered."

The Effect of Increased Temperature

"A marked acceleration in time of response was noted in
temperatures up to and including 25 degree C. The frog moved immediately and
directly from the darker end of the box to the lighted end where it remained
close to the glass. Between 25 and 30 degrees C the frog became restless and
moved about much. Above 30 degrees C movements toward the darker end were
as frequent as those toward the lighter end."

The Effect of Lowered Temperature

In a test box at 8 degrees C.

"When a
frog was placed in its rear end, head turned from the light, it moved to the
light at once, remained there for one-half minute, but retreated, turned away
from the light, and remained in the rear of the box, either moving about,
its head down as if it were trying to get under something, or quietly crouching,
with the head down during the other nine and one-half minutes of the experiment.
When returned to the aquarium (15 degrees C.), the above movements continued
in the water, the frog remaining for several minutes on the floor of the aquarium.
Five frogs were tried; three of these did not leave the rear end of the box
at any time."

The normal response of frogs to low temperature is to find a hiding
place, preferably under water, were it can rest until warmer temperatures
return. The above experiment clearly shows the change in strategic actions
due to lower temperatures.

Will this Type of Frog Burrow Under Sand During Cold Temperatures?

Several inches of sand was placed at the bottom of a large water
filled jar.

"Twelve frogs were tried. When the temperature of the water in the
jar became 10 degrees C. the frogs went down and remained down, with the body flat
and limbs outspread, but no attempt was made to burrow. The crouching movements,
together with the passing of the head over the surface of the sand as if exercising
a sense of touch, continued with a lowering of the temperature to 4 degrees
C, when they ceased. When a rock was lowered into the jar in such a way that
a small space was formed between it and the wall of the jar, the frog crawled
into this space and remained there. When a space was formed between the bottom
of the jar and the rock, it crawled into that. This was tested several times."

How Does a Frog Recognize a Shadow?

"The side of a large wooden box was covered
with black cloth and the frog placed near the black perpendicular surface.
It hopped close to this remained but a couple of minutes, then moved tot he
wall of the gray-colored building, where it remained at rest in the angle
formed by the wall and the ground. When placed near the uncovered box ...
there was no movement towards it. When the box was raised on one edge and propped
so that the other edge was about four inches from the ground, the frog moved
toward the shadow thus formed, crept well under the box, placed the body between
its floor and the ground, where it remained with its head directed outward."

"A black cloth was fastened close to the ground in the center of a sun illuminated
area, and a frog placed near it moved onto it, crept along the edge as if
seeking cover, then hopped off. A second frog also hopped onto the cloth,
but almost immediately moved off."

"Tests were also made at mid-day on a level
tract of ground about two acres in extent which contained neither trees nor any
object that could cast a shadow. Six frogs were tried. When freed, each moved
indifferently toward any point of the compass, but usually kept on moving
in the direction in which it began to move. In several trials no movement
resulted: the frog crouched low between short bunches of grass, its head held
close to the ground."

"Playing Dead" as another Type of Strategic Action

Curtis Riley (1913) at the University of Illinois reported that the toads
(Bufo Americanus) with which he was working exhibited a "playing dead" response
to rough handling. This response may be triggered by the motion sensors of the
inner ear. He describes it this way (page 201):

"The legs are drawn up closely against
the body and they assume a more or less rigid condition, the animal remaining
motionless. Sometimes a toad lies so absolutely quiet that even the respiratory
movements are unobserved, and the eyes may be closed. A young toad may be
made to feign death by being placed on its back in the hand or on the laboratory
table, and held in that position for a few seconds."

"There is considerable
variation among different individuals regarding the length of time of the
death-feigning response. Some feign death for a few seconds only, while others
retain the death-feigning posture for a minute and occasionally even for a
longer time."

Mature specimens of Bufo americanus will also feign death if they
are held upside down for approximately 30 seconds, a longer amount of time than
is needed for young toads. The frog Rana pipiens can also be made to feign
death.

Minimizing Aversive Cost

If a frog is given a light cue it can learn to avoid
responding (jumping) to a mild shock while still responding to a large shock.
This is significant for in classical conditioning learning an animal
would use the light cue to initiate an escape before the shock occurred. The extent
of this light inhibition is described by Robert Yerkes (1904 - page 127):

"The inhibitory influence of light in this case depends upon the intensity
of the electric stimulus. Even a very strong light will not cause much retardation
to a 3 or 4 cell current. As the strength of the electric stimulus decreases
the delay of reaction increases, until finally there is complete inhibition. At
this point an electric stimulus to which the frog would react almost invariably
when there is no disturbing condition will fail to cause reaction in the presence
of a sudden increase in light intensity."

(If the battery cells back then
are similar to the cells of today each one produces 1.5 volts so 3 to 4 cells
connected in series would produce 4.5 to 6 volts)

Table 1 shows how one frog learned
to stop responding to the mild shock. The learning was quick yet the frog
still occasionally tested whether the shock still occurred by temporarily
"forgetting" the association. Table 2 shows the reactions of the same frog
a half hour later. It still responds to mild shocks when no preceding light
cue is provided but immediately stops when the cue is provided once again.
Notice the wide variation in response times. (One wonders if this wide variation
would hold with stronger shocks.)

Significantly, the frogs tested by Yerkes
were not able to use the sound from an electric bell as a cue indicating that frog
brains are not "wired" to make this association.

The frogs in this series
of experiments seem to be comparing the aversiveness of its jumping reaction
to the aversiveness of the shock. If the shock is mild enough the frog ceases to
respond. This minimization of aversive cost is most likely the function of
the forebtain’s septum and amgdala. ( A great experiment would be to remove the
brain regions and then determine if the shock response can still be inhibited).

Reaction Time of Frog to One Celled Electric Shock Preceded by a Light Cue 2 Seconds Before Shock

Trial Number

Reaction Time (ms)

1

144

2

192

3

587

4

No Reaction

5

No Reaction

6

Reaction to 2nd Stimulus

7

No Reaction

8

No Reaction

9

177

10

No Reaction

11

No Reaction

12

No Reaction

13

1190

14

No Reaction

Table 1

Reaction Time of Light Trained Frog to One Celled Electric Shock

Trial Number with no Light Cue

Reaction Time (ms)

1

152

2

145

3

221

4

327

5

263

6

271

7

329

8

215

9

225

10

216

11

No Reaction

Trial Number with Light Cue

-----

11

No Reaction

12

No Reaction

13

No Reaction

14

No Reaction

15

No Reaction

Trial Number with no Light Cue

-----

16

216

Table 2

References

Burnett, Theodore C. (1912) Some Observations of Decerebrate
Frogs with Special Reference to the Formation of Associations, American
Journal of Physiology 30:80-87

Riley, C.F. Curtis (1913) Responses of Young Toads
to Light and Contact. The Journal of Animal Behavior 3:179-214

Web site by David D. Olmsted. He
can be contacted at brainsim1-contact at yahoo dot com (this is an anti-spam tactic.
Type the address as normal). Original site established
August 21, 1998 by David D. Olmsted. New home page
published August 25, 2006